A Biodegradable Formulation for Lacewings to Trigger Biological Control of Aphids
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insects Article Recruiting on the Spot: A Biodegradable Formulation for Lacewings to Trigger Biological Control of Aphids Joakim Pålsson 1,†, Gunda Thöming 2,†, Rodrigo Silva 3, Mario Porcel 1,‡ , Teun Dekker 1 and Marco Tasin 1,* 1 Department of Plant Protection Biology, Swedish University of Agricultural Science, 230 53 Alnarp, Sweden; [email protected] (J.P.); [email protected] (M.P.); [email protected] (T.D.) 2 NIBIO, Norwegian Institute of Bioeconomy Research, Postbox 115, NO-1431 Ås, Norway; [email protected] 3 Isca Technologies Inc., 1230 Spring St., Riverside, CA 92507, USA; [email protected] * Correspondence: [email protected]; Tel.: +46-40-415320 † Shared First Authorship. ‡ Current address: Corporación Colombiana de Investigación Agropecuaria (Agrosavia), C. I. La Libertad, Vía Puerto López km 17, Meta, Colombia Received: 28 November 2018; Accepted: 29 December 2018; Published: 5 January 2019 Abstract: Upon herbivory, plants release herbivore-induced plant volatiles (HIPVs), which induce chemical defenses in the plant as well as recruit natural enemies. However, whether synthetic HIPVs can be employed to enhance biological control in a cultivated crop in the field is yet to be explored. Here we show that a biodegradable formulation loaded with induced and food-signaling volatiles can selectively recruit the common green lacewing, Chrysoperla carnea, and reduce pest population under field conditions. In apple orchards, the new formulation attracted lacewing adults over a 4-week period, which correlated well with independent assessments of the longevity of the slow-release matrix measured through chemical analyses. In barley, lacewing eggs and larvae were significantly more abundant in treated plots, whereas a significant reduction of two aphid species was measured (98.9% and 93.6% of population reduction, for Sitobion avenae and Rhopalosiphum padi, respectively). Results show the potential for semiochemical-based targeted recruitment of lacewings to enhance biological control of aphids in a field setting. Further research should enhance selective recruitment by rewarding attracted natural enemies and by optimizing the application technique. Keywords: apple; barley; Chrysoperla carnea; herbivory induced plant volatiles; integrated pest management; semiochemicals; ecological intensification 1. Introduction Intensification of food production has been at odds with ecological sustainability. Among the unintended side effects are the loss of biodiversity, the simplification of the landscape, and an increased reliance on pesticides [1]. While these production systems favor high yields, corresponding repercussions on multitrophic relationships, such as pest’s natural enemy interactions, have been significant [2]. Ecological intensification is proposed as an approach to restore multifunctionality in agro-ecosystems, while supporting high productivity levels [3]. Enhancing biological control of insect pests through ecological processes is among the objectives of the “ecological paradigm shift” [3]. While an increasing body of evidence demonstrates how botanical diversity can effectively prevent pest attacks in crops by re-establishing trophic cascades [4], practical knowledge and cultural and economic gaps often impede the adoption of this concept in both high and low-input agricultural systems [5,6]. New methods should thus be developed to gradually transit from current input intensive monoculture to ecologically intensified crops. Insects 2019, 10, 6; doi:10.3390/insects10010006 www.mdpi.com/journal/insects Insects 2019, 10, 6 2 of 15 Plants developed chemical and physical defenses to counter herbivory, some of which are only expressed upon attack. These inducible defense mechanisms can be particularly advantageous when herbivores are diverse and variable in time and space, and allow plants to optimize resource allocation and tailor the response to the current threats [7]. Among inducible defenses, herbivory-induced plant volatiles (HIPVs) rapidly prime surrounding tissue and neighboring plants and recruit natural enemies from a distance. In order to induce systemic defense in the whole plant, HIPVs are released from the damaged area into the atmosphere [8,9]. A faster induction at the individual plant level may be achieved through the atmosphere, especially in large plants such as trees. HIPVs additionally allow the releasing plant to communicate with other trophic levels, attracting predators and parasitoids [10]. As the emission of HIPVs occurs exclusively upon herbivory, they provide an honest cue to both specific and generalist third trophic level arthropods. Given such properties, synthetic HIPVs may be used as a tool for pest management in agriculture [11]. Several suggestions on how to utilize HIPVs in crops are reported in literature, either as a way of monitoring beneficial arthropods within a crop or to attract natural enemies in an attempt to directly control pest populations [12]. Indeed, HIPVs have been found to attract natural enemies belonging to different families, including hoverflies (Diptera: Syrphidae), predatory bugs (Heteroptera), ladybirds (Coleoptera: Coccinellidae), predatory mites (Mesostigmata), parasitic wasps (Hymenoptera), and green lacewings (Neuroptera: Chrysopidae) [11]. Because the composition of the volatile blend was found to fine-tune the range of attracted natural enemies, information on possible synergies among volatiles with a diverse ecological function could be used to specifically modulate behaviors of such beneficial arthropods [13]. For example, acetic acid (AA), which is often considered a sugar signaling compound, enhanced attraction of a number of insect species to plant volatiles [14,15]. Similarly, phenylacetaldehyde (PAA), which is a nectar-signaling floral as well as an induced volatile [16,17], was reported to increase predator attraction when added to other plant volatiles [16]. The synergy between food-signalling cues and classical inducible compounds, such as methyl salicylate (MS), which is attractive for several predatory groups [18], may be particularly interesting in species where biological control is not directly exerted by the attracted adults, but rather by their offspring. One such biological control agent is the common green lacewing, Chrysoperla carnea s.l., adults of which feed on nectar and pollen, while the larvae are generalist predators [19]. Several compounds attracted significant amounts of lacewings (i.e., Acetophenone, 2-phenylethanol (PE), PAA) in cherry, apricot, apple, pear, and walnut orchards [16,20,21]. Interestingly, a blend of MS, PAA, and AA not only attracted adults, but was also capable of increasing the oviposition rate in the vicinity of the releasing point, possibly thanks to the presence of food signalling volatiles [22]. In addition, this blend significantly increased lacewing density in overwintering boxes [22]. Whether this blend is capable of enhancing pest control in the surrounding vegetation remains to be investigated. We hypothesized that a novel formulation consisting of plant and food odors embedded in a biodegradable matrix can attract lacewing from surrounding vegetation and induce oviposition on the plant. We further hypothesized that this recruitment of adults would contribute to the suppression of aphid populations. Common green lacewing attraction from a distance and release of volatiles from emitting devices were evaluated in apple orchards (Malus domestica Borkhausen). However, the assessment of biological control was carried out in a cereal field, due to a higher and much more homogeneous pest attack in comparison to orchards. Parameters such as larval lacewing density and population level of other natural enemies were measured in the system of barley (Hordeum vulgare L.), two hemipteran herbivores, Sitobion avenae (F.) and Rhopalosiphum padi (L.), and the common green lacewing as a generalist predator. In order to propose a method with a low environmental impact, we compared the efficacy of a standard polyethylene-based bag odor dispenser with a newly assembled prototype based on a biodegradable matrix. Insects 2019, 10, 6 3 of 15 2. Materials and Methods 2.1. Volatile Releasing Formulations The reference device was purchased from Csalomon (Plant Protection Institute, MTA ATK, Budapest, Hungary). It consisted of a cotton wick loaded with a 3-component blend of MS, PAA, and AA in a 1:1:1 ratio with a total load of 300 mg/device. The wick was placed into a sealed polyethylene bag, through which volatiles were slowly released (hereafter referred to as PE bag). In order to facilitate its use in the field, this device was delivered with a pre-attached plastic strip to be stapled into the canopy, or to a holding stick. We selected this formulation as a benchmark because field data on lacewing attraction and oviposition using this formulation were available at the time of our study [20]. The new formulation was a novel product prepared in co-operation with ISCA Technologies (ISCA Technologies Inc., Riverside, CA, USA) and Bio-Innovate AB (Lund, Sweden). It consisted of a biologically inert, biodegradable wax-water emulsion releasing paste loaded with the above-described blend at a concentration of 300 mg/mL. A single release point for this product constituted a 1 mL droplet applied with a plastic syringe (hereafter referred to as paste). Data on the slow-release properties of the paste using other volatile cues are also available [23]. 2.2. Measurement of Volatile Release To compare over time the volatile release